PsbS as a Conserved Regulator of Non-photochemical Quenching Across Green Lineage Evolution

Abstract Excess light during photosynthesis induces harmful reactive oxygen species. As a defense mechanism, plants possess rapidly reversible energy-dependent quenching (qE), in which excitation energy in the photosystem II antenna is dissipated as heat when absorbed light is in excess. In the Viridiplantae, qE is regulated by two key proteins: LHCSR and PsbS. LHCSR is widely conserved in green algae and bryophytes, early-diverging land plants. In contrast, PsbS functions as the major qE regulator in vascular plants, reflecting an evolutionary shift from LHCSR to PsbS. Despite its importance in vascular plants, the function of PsbS remains poorly understood in green algae, especially in streptophyte algae, the closest relatives of land plants. To examine PsbS activity in streptophyte algae, we focused on Chlorokybus cerffii and Klebsormidium nitens, which represent early-diverging lineages in Streptophyta. We expressed their PsbS genes in the PsbS-deficient Arabidopsis thaliana mutant npq4, along with PsbS genes from A. thaliana and Chlamydomonas reinhardtii. All PsbS genes complemented the npq4 mutant phenotype with varying degrees of efficiency depending on the protein expression levels. Moreover, the qE efficiencies per unit of PsbS protein in the algal PsbS transformants were equal to or higher than those of AtPsbS transformants. The results suggest that PsbS activity as a qE regulator was already established in the common ancestor of streptophytes prior to land plant colonization.